Diapause Characteristics of the Taiwanese Populations of Tetranychus kanzawai Kishida and T. urticae Koch (Acari: Tetranychidae)

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1 , Diapause Characteristics of the Taiwanese Populations of Tetranychus kanzawai Kishida and T. urticae Koch (Acari: Tetranychidae) Akio Takafuji 1 *, Norihide Hinomoto 2, Chain-Ing T. Shih 3, Tetsuo Gotoh 4, Chyi-Chen Ho 5 and Chien-Chih Wang 3 1. Laboratory of Ecological Information, Graduate School of Agriculture, Kyoto University, Kyoto , Japan 2. National Institute of Agrobiological Sciences, Tsukuba, Ibaraki , Japan 3. Department of Entomology, National Chung-Hsing University, Taichung 40227, Taiwan (ROC) 4. Laboratory of Applied Entomology and Zoology, Faculty of Agriculture, Ibaraki University, Ami, Ibaraki , Japan 5. Applied Zoology Division, Agricultural Research Institute, Council of Agriculture, Wufeng, Taichung 41301, Taiwan (ROC) (Accepted for publication: May 9, 2005) ABSTRACT Takafuji, A.*, Hinomoto, N., Shih, C. I. T., Gotoh, T, Ho, C. C., and Wang, C. C Diapause characteristics of the Taiwanese populations of Tetranychus kanzawai and Tetranychus urticae (Acari: Tetranychidae). Plant Prot. Bull. 47: We studied the diapause percentages of Tetranychus kanzawai Kishida and T. urticae Koch populations derived from various regions of Taiwan, at three temperatures under a day-length of 9 h. The T. kanzawai populations of Taiwan exhibited various diapause percentages, which were lower than those of populations from Kagoshima, southern Kyushu, Japan, but were much higher than those from the Okinawa islands southernmost of Japan. The diapause percentages were not clearly correlated with the latitudes or altitudes from which the populations were derived. This result implied that * Corresponding author. takafuji@kais.kyoto-u.ac.jp

2 the Taiwanese T. kanzawai originates from immigrants from various regions outside Taiwan. On the other hand, all populations of T. urticae of Taiwan showed a very low incidence of diapause, like the populations in warm areas of Japan. This suggested that both Taiwanese and Japanese populations had the same origin. (Key words: Diapause, Tetranychus kanzawai, Tetranychus urticae, Taiwan) INTRODUCTION The spider mites (Tetranychidae), Tetranychus kanzawai Kishida and T. urticae Koch, are serious, polyphagous pests in eastern Asia, such as Japan, Taiwan, Korea and China (1). T. kanzawai has also become abundant recently in South-east Asia (Takafuji, personal observation). Based on the morphological and molecular analyses, as well as crossing experiments, Navajas et al. (4) revealed that T. hydrangeae, which mainly occurs on Hydrangea spp., is synonymous with T. kanzawai, and then T. kanzawai has a wider distribution range than it had previously been thought. Now the mites have been recorded worldwide probably due to immigration (3). Navajas et al. (4) suggested that the mites originated in South-east Asia but without any explicit evidence and analysis. Contrary to their inference, our observations show that T. kanzawai is not very common in tropical South-east Asia and the mites seem to occur only on agricultural crops. We seldom find them on wild plants, implying that the mites did not originate from tropical South-east Asia. In Japan, T. kanzawai is a serious pest commonly distributed all over the country, and maintains its population on a variety of wild plants, as well as on cultivated crops (5, 6). This is also the case in the temperate regions of China (Takafuji, personal observation). In Taiwan, T. kanzawai is currently one of the most common spider mites, occurring on various host plants including tea (7, 8, 9), although it is believed that the mites are exotic and invaded Taiwan in 1960 s (7). It is not unknown, however, where the mites originated from. On the other hand, molecular phylogenetic analyses by Navajas (10), Navajas et al. (2) and Hinomoto et al. (11) strongly suggested that T. urticae originated in the Mediterranean regions and diverged into two distinct lineages, one of which extended its distribution range worldwide. T. urticae (green form) used to be abundant only in northern Japan before the late 1970 s but thereafter expanded its distribution to the south (12). However, T. urticae is a serious pest only on horticultural crops under highly artificial conditions such as in glasshouses and orchards. Under natural conditions the mites are rarely found and are localized in southern Japan. A similar trend is also seen in Taiwan. As in several Tetranychus species, both T. kanzawai and T. urticae undergo a reproductive diapause mainly induced by short-days and low temperatures. The majority of populations on the four main islands of Japan exhibit more than 90% diapause at 15 C under a day-length of 9 h.

3 Diapause of Taiwanese Populations of T. kanzawai and T. urticae 105 Even the populations from Kagoshima Prefecture (southern Kyushu) have a high diapause capacity and only populations on the Okinawa islands (southernmost islands of Japan) have a very low capacity for diapause (5). We previously reported (9) that populations from West-central Taiwan, located in slightly lower latitudes than the Okinawa islands, had a wide range of diapause percentages and even some populations at lowlands showed as high a diapause capacity as those in southern Honshu, Japan. This fact indicated that T. kanzawai in Taiwan have genetically diversified diapause characteristics. On the other hand, diapause percentage of Japanese T. urticae showed a clinal decrease with decreasing latitude and populations in the West-central and southern Japan had a very low capacity for diapause (13). Populations in west-central Taiwan also had a low diapause capacity (9). We continued the previous study (9) on the diapause characteristics of the Taiwanese populations of the two species, including those from southern and northern Taiwan to elucidate the diapause characteristics of the two spider mites in Taiwan. This is the third of our series of studies on the diversification of adaptive traits such as diapause and in molecular analysis-based phylogenetic studies for populations in eastern and South-east Asia, to elucidate the process in the distribution expansion of the two spider mite species mentioned above. MATERIALS AND METHODS Mites We collected 24 populations of T. kanzawai (Table 1) and 11 populations of T. urticae (green form) (Table 2) from various regions in Taiwan and various host plants at three time points: mid-december 1999, late September 2000 and late November These populations were collected from latitudes ranging from about 22 to 25 N and from altitudes ranging from about 10 to 800 m. We have not attempted collecting populations from altitudes higher than 1000 m. Host plant leaves with mites were collected and put into paper bags wrapped with plastic ones. We carried them to Japan preserved in a cooling box. We did not use collected samples comprised of less than 10 adult females for diapause experiments to avoid a bottleneck effect. Collected mites were then reared for one or two generations on detached kidney bean (Phaseolus vulgaris L.) leaves at 25 C under a 16L8D photoperiod to obtain enough adult females for the experiments. Species were identified by T. Gotoh. Diapause We transferred more than 30 adult females (most of them should have already mated) randomly chosen from each local culture of each of the two species onto four detached bean leaves pressed on top of water-saturated cotton in 9-cm Petri dishes. All four dishes for each population were kept together in a transparent plastic container with a hole (15 cm diameter) covered with nylon cloth for ventilation. Thus the relative humidity inside the container was maintained between 70 and 90 % RH.

4 Table 1. Collection records and the % diapause in Tetranychus kanzawai populations in Taiwan 1) Popu- Site % Diapause (n) Altitude lation Code Prefecture City Latitude Date Host plant (m) 15 C 18 C 20 C (Town) (N) FK1 Taipei Pinglin 24 93' 29 Nov Tea 73.7 (494) 80.0 (529) 4.8 (272) FK2 Nantou Minjian 23 50' 14 Dec Tea 75.9 (266) 75.5 (440) 31.3 (201) FK3 Nantou Minjian 23 50' 14 Dec Tea 80.9 (944) 53.5 (484) 34.8 (457) FK4 Nantou Lugu 23 40' 14 Dec Tea 82.2 (1219) 56.4 (981) 30.9 (1551) FK5 Nantou Lugu 23 40' 22 Sep Tea 99.7 (596) 98.8 (400) 13.0 (517) FK6 Nantou Lugu 23 40' 22 Sep Tea 87.0 (338) 53.4 (354) 6.1 (293) FK7 Nantou Lugu 23 40' 22 Sep Peach 42.5 (426) 40.7 (519) 9.0 (597) FK8 Nantou Minjian 23 50' 14 Dec Cassava 45.5 (308) 25.1 (341) 0.8 (708) FK9 Nantou Minjian 23 50' 14 Dec Balloonvine 76.2 (604) 69.0 (588) 18.2 (313) FK10 Nantou Minjian 23 50' 21 Sep Sponge cucumber 68.4 (316) 47.2 (481) 3.1 (424) FK11 Taichung Dungshr 24 15' 19 Sep Pear 87.9 (544) 82.8 (586) 8.7 (575) FK12 Taichung Dungshr 24 15' 19 Sep Pear 34.0 (1092) 34.0 (762) 2.7 (1124) FK13 Taichung Dungshr 24 15' 19 Sep Cassava 73.1 (186) 58.8 (342) 2.1 (336) FK14 Changhua Datsuen 23 59' 20 Sep Pear 74.7 (403) 74.6 (587) 0.9 (465) FK15 Changhua Shihu 23 57' 20 Sep Peach 99.0 (1110) 97.5 (1157) 56.5 (978) FK16 Miaoli Miaoli 24 33' 19 Sep Pear 95.7 (515) 89.5 (569) 0 (637) FK17 Miaoli Miaoli 24 33' 19 Sep Pear 62.8 (736) 73.7 (778) 10.0 (689) FK18 Miaoli Miaoli 24 33' 15 Dec Strawberry 89.1 (339) 81.8 (539) 30.4 ( 73) FK19 Pingtung Gunshu 22 47' 27 Nov Phaseolus sp (221) 59.2 (591) 6.4 (547) FK20 Pingtung Gunshu 22 47' 27 Nov Cassava 72.4 (458) 29.9 (670) 3.4 (547) FK21 Kaohsiung Maulin 22 51' 27 Nov Cassava 0.7 (272) 14.0 (443) 0.8 (364) FK22 Kaohsiung Meinung 22 51' 27 Nov Sponge cucumber 49.0 (306) 19.1 (529) 12.7 (604) FK23 Kaohsiung Meinung 22 51' 27 Nov Eggplant 28.0 (418) 44.6 (747) 0 (548) FK24 Taitung Luye 22 56' 28 Nov Tea 62.0 (208) 12.1 (429) 9.9 (202) 1) Tea: Camellia sinensis, Peach: Prunus persica, Cassava: Manihot esculenta, Balloon-vine: Cardiospermum halicacabum, Sponge cucumber: Luffa cyclindrica, Pear: Pyrus serotina, Strawberry: Fragaria chiloensis Duch.var. ananassa, Eggplant: Solunum melongena. Table 2. Collection records and the % diapause of Tetranychus urticae in Taiwan 1) Popu- Site % Diapause (n) Altitude lation City Latitude Date Host plant Prefecture (m) 15 C 18 C 20 C code (Town) (N) FU1 Miaoli Miaoli 24 35' 15 Dec Strawberry 0.2 (604) 0 (314) 0 (416) FU2 Miaoli Miaoli 24 35' 15 Dec Strawberry 2.8 (528) 0.5 (762) 0 (487) FU3 Miaoli Miaoli 24 35' 15 Dec Strawberry 5.7 (316) 0 (307) 0 (446) FU4 Miaoli Dahu 24 33' 29 Nov Strawberry 0 (177) 0.4 (249) 0 (250) FU5 Miaoli Dahu 24 33' 29 Nov Kidney bean 1.1 (185) 0 (436) 0 (324) FU6 Changhua Tianwei 23 53' 21 Sep Chrysanthemum ) 0 (308) 0 (450) FU7 Changhua Tianwei 23 53' 21 Sep Chrysanthemum 0.4 (269) 0 (344) 0 (348) FU8 Changhua Tianwei 23 53' 21 Sep Chrysanthemum 20.9 (474) 0 (344) 0 (348) FU9 Taichung Dungshr 24 15' 19 Sep Pear 0 (209) 0 (319) 0 (284) FU10 Pington Pingtung 22 39' 27 Nov Rose 0.4 (217) 0 (271) 0 (265) FU11 Taitung Taitung 22 57' 28 Nov Rose 0 (388) 0 (165) 0 (396) 1) Strawberry: Fragaria chiloensis Duch.var. ananassa, Kidney bean: Phaseolus vulgaris, Chrysanthemum: Callistephus chinensis, Pear: Pyrus serotina, Rose: Rosa hybrida.

5 Diapause of Taiwanese Populations of T. kanzawai and T. urticae 107 Fig. 1. Diapause percentage of Tetranychus kanzawai populations from Taiwan, at 15 C-9L15D. We allowed females to lay eggs for 2-3 days at 25 C -16L8D, and then removed them. The offspring were reared at 15, 18 or 20 C under a day-length of 9 h to determine the incidence of diapause (see (14, 15) ). We examined the diapause status of females 7 to 10 days after adult emergence. More than 95% of females (n = from 4 randomly chosen populations) that had an orange body color did not lay any eggs at least three days following a period of 7-10 days post-maturation under the rearing conditions of the offspring; therefore they were judged to have entered diapause. RESULTS As we reported previously (9), the

6 Taiwanese populations of T. kanzawai showed a variety of diapause incidences, in particular, at 15 and 18 C (Figs. 1 and 3 (upper); Table 1). At 15 C some populations had more than 90% diapause, whereas others showed very low diapause percentages (Fig. 3; upper). At all three temperatures the diapause percentages of the Taiwanese populations of T. kanzawai were significantly lower than those from the Kagoshima populations (see (9), Scheffe s method: p = at 15 C, p = at 18 C and p < at 20 C). However, they were much higher than those from the Okinawa Islands (see (9) ). There was a significant (P = 0.002) decrease in diapause percentage with decreasing latitude only at 18 C (Fig. 4); some of the populations in southern Taiwan (FK21 and FK23) tended to show lower incidence of diapause but the southern populations also had a variety of diapause percentages, as was observed in populations in West-central regions. In Taiwan, T. kanzawai is distributed over a wide range of Fig. 2. Diapause percentage of Tetranychus urticae populations from Taiwan, at 15 C-9L15D.

7 Diapause of Taiwanese Populations of T. kanzawai and T. urticae 109 altitudes. However, populations in West-central regions (FK2 - FK18) derived from various altitudes did not show any significantly increased diapause percentage at all with increasing altitude (Fig. 6), although we have not studied populations at very high latitudes. For example, a population derived from 800m in altitude (FK6) had a very high incidence of diapause but also one from a very low altitude (FK15) showed a high diapause percentage similar to that of FK6 (Table 1). In the populations from the West-central regions, no significant difference was observed between populations derived from tea and those from non-tea hosts (t-test: p = at 15 C, p = at 18 C and p = at 20 C). On the other hand, populations from southern Honshu (Japan) tended to have a slightly lower diapause capacity than those from deciduous and herbaceous hosts (5). Fig. 3. The diapause incidence of Tetranychus kanzawai (top) and T. urticae (bottom) populations from Taiwan, at three temperatures with a day-length of 9 h.

8 Fig. 4. Relationship between the diapause percentages of Tetranychus kanzawai populations collected from Taiwan and the latitudes where they were collected. The diapause percentages were described by arcsine transformation. By regression analysis, y = x and r = (p = 0.059), y = x and r = (p = 0.002), and y = x and r = (p = 0.714), were obtained for 15 C, 18 C and 20 C, respectively (see Fig. 3). Fig. 5. Relationship between the diapause percentages of Tetranychus urticae populations collected from Taiwan and the latitude where they were collected. The diapause percentages were described by arcsine transformation. By regression analysis, y = x and r = (p = 0.979), and y = x and r = (p = 0.243) were obtained for 15 C and 18 C, respectively.

9 Diapause of Taiwanese Populations of T. kanzawai and T. urticae 111 Fig. 6. Relationship between the diapause percentages of Tetranychus kanzawai population collected from west-central Taiwan and the altitudes where they were collected. The diapause percentages were described by arcsine transformation. By regression analysis, y = x and r = (p = 0.882), y = x and r = (p = 0.494), and y = x and r = (p = 0.557), were obtained for 15 C, 18 C and 20 C, respectively. Fig. 2 illustrates the geographical distribution of the diapause percentage and Fig. 3 (bottom) shows the incidence of diapause at three temperatures, of T. urticae (see also Table 2 for more details). Diapause capacity was very low in all populations. At 20 C none of the populations expressed diapause, although the mites genetically maintained a diapause trait, as some individuals comprising each population expressed diapause at 15 C. No significant decrease in diapause percentage was observed with decreasing latitude at all three temperatures (Fig. 5). This low diapause characteristic of T. urticae is common to the populations in lower latitudes of Japan (5). DISCUSSION T. kanzawai in Taiwan consisted of populations with various capacities for diapause. The diapause characteristics in the Taiwanese populations are different from those of populations on the main islands of Japan (5) and temperate areas in China (Takafuji, unpublished), most of which exhibited high diapause incidences, and also different from those of populations on the Okinawa Islands having a very low diapause capacity (5). One hypothesis for the diversified diapause characteristics in the Taiwanese populations of T. kanzawai will be that they would have originated from immigrants from various regions of the world, where original populations had various diapause characteristics. Winter in Taiwan, except at highlands, is fully tolerable for the survival of over-wintering T. kanzawai. The average temperature in winter of Taichung (West-central Taiwan) is over 15 C at which

10 diapause can be induced in the populations in the winter if the mites genetically have the capacity. However, they should be able to over-winter successfully without entering diapause, unless plant conditions heavily deteriorate. Our field observations in midand late December in tea fields at West-central Taiwan confirmed that the body color of a proportion of adult females had turned orange, showing that they would be in diapause. This fact implies that the selective pressure derived from the warm winter conditions in Taiwan would not have significantly acted in favor of the non-diapause trait, the diapause trait being maintained in the populations. Another explanation for the variations is that there is a frequent gene flow occurring between populations at very high and lower altitudes. This gene flow may be attributed to the maintenance of diapause capacity. However, we have not studied the diapause characteristics at very high elevations, and have not confirmed any gene exchange between low and high altitudes. In contrast to T. kanzawai, even populations in South-west Honshu, Japan of T. urticae have a very weak diapause capacity (13). Thus, all populations from Taiwan and lower latitudes of Japan, including Okinawa Islands have a similar, low diapause capacity. This similar characteristic conforms to the phylogenetic study that the Taiwanese and Japanese populations belong to the same linage (11). ACKNOWLEDGMENTS We wish to express our sincere appreciation to Messrs Y. Y. Chuang, K. F. Pai and C. H. Shaw for helping us collect mite samples and Dr. S. Santoso for his help in the experiments. This study was supported in part by Grants-in-aid for Scientific Research Nos. (B) ( and ) from the Ministry of Education, Culture, Sports and Technology, Japan, to A. Takafuji. LITERATURE CITED 1. Ehara, S Revision of the spider mite family Tetranychidae of Japan. Species Diversity 4: Navajas, M., Lagnel, J., Gutierrez, J. and Boursot, P Species-wide homogeneity of nuclear ribosomal ITS2 sequences in the spider mite Tetranychus urticae contrasts with extensive mitochondrial COI polymorphism. Heredity 80: Bolland, H. R., Gutierrez, J. and Flechtmann, C. H. W World catalogue of the spider mite family (Acari: Tetranychidae), with reference to taxonomy, synonymy, host plant and distribution.brill, Boston. 384 pp. 4. Navajas, M., Gutiterrez, J. and Gotoh, T Synonymy between two spider mite species, Tetranychus kanzawai and T. hydrangeae (Acari: Tetranychidae), shown by ribosomal ITS2 sequences and cross-breeding experiments. Bull. Entomol. Res. 91: Takafuji, A., Santoso, S., and Hinomoto, N Host-related differences in diapause characteristics of different geographical populations of the Kanzawa spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae). Appl.

11 Diapause of Taiwanese Populations of T. kanzawai and T. urticae 113 Entomol. Zool. 36: Takafuji, A, and Morishita, M Overwintering ecology of two species of spider mites (Acari: Tetranychidae) on different host plants. Appl. Entomol. Zool. 36: Ho, C. C An introduction to the exotic mite pests in Taiwan. Chinese J. Entomol., Special Publ. 2: Ho, C. C Spider-mite problems and control in Taiwan. Exp. Appl. Acarol. 24: Takafuji, A., Santoso, S., Hinomoto, N., Shih, C. I. T., and Gotoh, T Diapause characteristics of two species of tetranychid mites (Acari: Tetranychidae) in southern Japan and Taiwan. Appl. Entomol. Zool. 38: Navajas, M Host plant association in the spider mite Tetranychus urticae (Acari: Tetranychidae): insights from molecular phylogeography. Exp. Appl. Acarol. 22: Hinomoto, N., Osakabe, M. H., Gotoh, T., and Takafuji, A Phylogenetic analysis of green and red forms of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), in Japan, based on mitochondrial cytochrome oxidase subunit I sequences. Appl. Entomol. Zool. 36: Gotoh, T. and Shinkaji, N Critical photoperiod and geographical variation of diapause induction in the two-spotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae), in Japan. Jpn. J. Appl. Entomol. Zool. 25: Takafuji A, So, P. M., and Tsuno. N Inter- and intra-population variations in diapause attribute of the two-spotted spider mite, Tetranychus urticae Koch, in Japan. Res. Popul. Ecol. 33: Lees, A. D Environmental factors controlling the evocation and termination of diapause in the fruit tree red mite Metatetranychus ulmi Koch (Acarina: Tetranychidae). Ann. Appl. Biol. 40: Goka, K., and Takafuji, A Genetical studies on the diapause of the two-spotted spider mite, Tetranychus urticae Koch (1). Appl. Entomol. Zool. 31:

12 Akio Takafuji 1 * Norihide Hinomoto 2 3 Tetsuo Gotoh 蟎 蟎 ( 1 Laboratory of Ecological Information, Graduate School of Agriculture, Kyoto University, Kyoto , Japan 2 National Institute of Agrobiological Sciences, Tsukuba, Ibaraki , Japan 3 4 Laboratory of Applied Entomology and Zoology, Faculty of Agriculture, Ibaraki University, Ami, Ibaraki , Japan 5 ) 採自台灣不同地區的神澤氏葉蟎 Tetranychus kanzawai 二點葉蟎 T. urticae 台灣神澤氏葉蟎表 葉蟎可能源自多 台灣二點葉蟎族群與日本較暖和地區的族群相似 此結果建議台灣及日本的二點葉蟎族群可能來自同源 ( Tetranychus kanzawai Tetranychus urticae ) * takafuji@kais.kyoto-u.ac.jp